What Currency Do Bumble Bees Maximize?

In modelling bumble bee foraging, net rate of energetic intake has been suggested as the appropriate currency. The foraging behaviour of honey bees is better predicted by using efficiency, the ratio of energetic gain to expenditure, as the currency. We re-analyse several studies of bumble bee foraging and show that efficiency is as good a currency as net rate in terms of predicting behaviour. We suggest that future studies of the foraging of bumble bees should be designed to distinguish between net rate and efficiency maximizing behaviour in an attempt to discover which is the more appropriate currency.     

Foraging behaviour and fuel accumulation of capital breeders during spring migration as derived from a combination of satellite‐ and ground‐based observations

The migration strategy of many capital breeders is to garner body stores along the flyway at distinct stopover sites. The rate at which they can fuel is likely to be strongly influenced by a range of factors, such as physiology, food availability, time available for foraging and perceived predation. We analysed the foraging behaviour and fuel accumulation of pink‐footed geese, an Arctic capital breeder, at their mid‐flyway spring stopover site and evaluated to what extent their behaviour and fuelling were related to physiological and external factors and how it differed from other stopovers along the flyway. We found that fuel accumulation rates of geese at the mid‐flyway site were limited by habitat availability rather than by digestive constraints. However, as the time available for foraging increased over the stopover season, geese were able to keep constant fuelling rate. Putting this in perspective, geese increased their daily net energy intake along the flyway corresponding to the increase in time available for foraging. The net energy intake per hour of foraging remained the same. Geese showed differences in their reaction to predators/disturbance between the sites, taking higher risks particularly at the final stopover site. Hence, perceived predation along the flyway may force birds to postpone the final fuel accumulation to the last stopover along the flyway. Flexibility in behaviour appears to be an important trait to ensure fitness in this capital breeder. Our findings are based on a new, improved method for estimating fuel accumulation of animals foraging in heterogeneous landscapes based on data obtained from satellite telemetry and habitat specific intake rates.     

经济学思想和方法在行为生态学中的应用

从经济学观点看,动物的任何一种行为都是一种投资,同时又能获得一定的收益。进化和自然选择将趋于使动物行为的净收益增至最大,这种思想也是组建行为生态学最适模型的基础。如果为海滨蟹提供各种大小不同的贻贝任其选食的话,那么它所选食的贻贝大小往往能使它得到最大的能量净收益。为了精确地计算捕食者应当吃多少不同大小的食物,就需要建立一个最适模型。当动物领域行为的收益大于投资时,自然选择就会促进这种行为的产生和发展,而最佳领域大小则可借助于建立经济模型进行预测。将饥饿风险降至最小的原则可应用于动物的觅食决策。绒斑啄木鸟在觅食时可利用它们所收集的信息使其食物摄取率达到最大。     

Optimal foraging in bumblebees: Calculation of net rate of energy intake and optimal patch choice

To test many predictions of “optimal foraging theory” it is necessary to calculate the rate of net energy intake of a foraging animal. Equations are derived for the calculation of the rate of net energy intake of a foraging bumblebee. The assumptions that form the basis of these energy equations are discussed. As examples, the rates of net energy intake are calculated for Bombus flavifrons workers foraging on neighboring patches of Aconitum columbianum and Delphinium barbeyi. If the bumblebees forage optimally, their net rates of energy intake in the two patches should be equal. The observed rates are consistent with this hypothesis. The application of an optimality approach to pollination biology is briefly discussed.     

Floral Temperature and Optimal Foraging: Is Heat a Feasible Floral Reward for Pollinators?

As well as nutritional rewards, some plants also reward ectothermic pollinators with warmth. Bumble bees have some control over their temperature, but have been shown to forage at warmer flowers when given a choice, suggesting that there is some advantage to them of foraging at warm flowers (such as reducing the energy required to raise their body to flight temperature before leaving the flower). We describe a model that considers how a heat reward affects the foraging behaviour in a thermogenic central-place forager (such as a bumble bee). We show that although the pollinator should spend a longer time on individual flowers if they are warm, the increase in total visit time is likely to be small. The pollinator's net rate of energy gain will be increased by landing on warmer flowers. Therefore, if a plant provides a heat reward, it could reduce the amount of nectar it produces, whilst still providing its pollinator with the same net rate of gain. We suggest how heat rewards may link with plant life history strategies.     

Honeybee (Apis mellifera ligustica) Response to Differences in Handling Time, Rewards and Flower Colours

Free flying honeybees were tested outdoors on blue–white and blue–yellow dimorphic artificial flower patches to examine the influence of reward difference, flower handling‐time difference and flower colour choice on foraging decisions. We employed different flower‐well depths to vary handling times (costs), and differences in sucrose molarity to vary reward quality. Tests were performed with 2 and 6 μl rewards to vary quantity. We show that when handling time is correlated with flower‐colour morphs on a pedicellate artificial flower patch, a honeybee's foraging behaviour is dependent on the flower colours used in the choice tests. This supports a honeybee foraging model where constraints are a significant factor in decision making. Bees visiting blue–yellow flower patches exhibited flower constancy to colour, where they restricted most visits to a single flower colour, some bees to blue and others to yellow, irrespective of handing time differences. When offered a choice of equally rewarding blue or white flowers, bees were not constrained by flower colour and chose to visit flowers with a lower handling time. When reward molarity varied with well depth between blue and white flowers, foragers chose shallow‐well flowers (short‐handling time) with a smaller net harvest rate over deep‐well flowers (long‐handling time) with a greater net harvest rate. Results using the blue–white dimorphic flower patch suggest that when foraging options simultaneously involve reward and handling‐time choices, honeybee forager behaviour is inconsistent with an absolute method of evaluating profit.     

Honeyeater foraging: A test of optimal foraging theory

Honeyeaters (Meliphagidae) were observed foraging for nectar from Lambertia formosa inflorescences, each of which has seven flowers. The frequency distribution of numbers of flowers probed per visit to an inflorescence was found to be bimodal, with one peak at two and the other at seven. It is hypothesized that this frequency distribution results from a rule of departure from inflorescences that maximizes the net rate of energy gain. Patterns of nectar distribution were determined for a large sample of inflorescences. In addition the extent to which the honeyeaters re-probe flowers during a visit to an inflorescence was estimated. From these data and from field measurements of the times required by the honeyeaters to perform the various foraging behaviours, computer simulations of honeyeater foraging were constructed. These simulations led in turn to optimal frequency distributions of numbers of flowers probed per inflorescence that were bimodal but had peaks at 1 and 7 instead of 2 and 7. Although the observed and predicted behaviour were consequently similar, the difference between them was nevertheless significant. This difference could have been due to the birds' transient occupancy of the study area.     

Foraging patterns and kleptoparasitism among three sympatric cormorants (Phalacrocorax spp.) from the Delhi region, North India

Cormorants, described as ‘foot-propelled pursuit divers’, constitute an important component of aquatic food webs and exhibit unique foraging behaviour patterns, which can be properly understood through a comparative study. Since, after a foraging dive they surface to ingest the prey, the intensity of kleptoparasitic attacks on the surface can have a major impact upon the net energetic gain for each individual. Inspite of the fact that cormorants and their habitats are severely threatened in India, their foraging behaviour has not been adequately studied. Such considerations prompted us to undertake field studies on three sympatric cormorants (Phalacrocorax spp.) at 60 different sites in the Delhi region of North India, during 2004–2007. By means of video photography, some key foraging parameters including group size, prey size and patterns of kleptoparasitic attacks were quantified. Along a loose body size gradient, we observed significant differences among the three species with respect to not only their preference for wetland size but also prey size. The frequency of a kleptoparasitic attacks depended upon the group size and foraging behaviour of each species. It was observed that several foraging bouts were abruptly terminated due to human disturbances, mostly at sites lying outside the protected areas. This observation points towards the need to conserve small waterbodies in the countryside, currently threatened by pollution and urbanization, for the benefit of a variety of waterbirds including cormorants.     

The cost of disturbance: a waste of time and energy?

Quantifying the effect of disturbance is a central issue in conservation. Using time and energy budgets, we obtain a range of ways to assess the importance of disturbance. One measure is the time that must be spent foraging in order to balance the energy budget. From this we derive critical levels of wastage (rate of disturbance multiplied by duration of disturbance) at which the animal runs out of time or reaches a limit on energy expenditure. In the case of the time constraint, the critical wastage is the net rate of energetic gain while foraging divided by the rate of energetic expenditure during a disturbance. The associated critical rate of disturbance is the net rate of energetic gain while foraging divided by the energy spent during a disturbance. The model is illustrated using data from the African wild dog, which suffers disturbance from lions and kleptoparasitism from hyenas. Findings suggest that disturbance imposes significant costs on wild dog time and energy budgets. We show how alternative environments can be evaluated in terms of their effective rate of gain, which is the net rate of gain from foraging minus the rate of energy expenditure as a result of disturbance.     

Evolutionary models of metabolism, behaviour and personality

I explore the relationship between metabolism and personality by establishing how selection acts on metabolic rate and risk-taking in the context of a trade-off between energy and predation. Using a simple time budget model, I show that a high resting metabolic rate is not necessarily associated with a high daily energy expenditure. The metabolic rate that minimizes the time spent foraging does not maximize the net gain rate while foraging, and it is not always advantageous for animals to have a higher metabolic rate when food availability is high. A model based on minimizing the ratio of mortality rate to net gain rate is used to determine how a willingness to take risks should be correlated with metabolic rate. My results establish that it is not always advantageous for animals to take greater risks when metabolic rate is high. When foraging intensity and metabolic rate coevolve, I show that in a particular case different combinations of foraging intensity and metabolic rate can have equal fitness.     

Influences of the season and the habitat structure on the foraging ecology of two coua species in the western dry forest of Madagascar

I studied the foraging ecology of Coquerel's Coua (Coua coquereli) and Giant Coua (Coua gigas), which occur in the dry forest in west Madagascar. This kind of forest is characterised by an alternating of a dry and a rainy season. The foraging behaviour was described in several dimensions: i.e. height and proportion of perching, rate of capture (estimating the food availability), foraging techniques, substrates used, type and size of the captured prey. Their foraging behaviour was different according to the season and to the proximity of water. Habitat structure was important to take in consideration to study their foraging behaviour. They tended to use the same pattern of techniques and substrates, but differed by the proportions they used these variables and also by the possibility to climb into the dense understorey vegetation. Seasonal variation has probably an important effect on the prey availability and the nature of prey captured. The diet of both species is also discussed. I suggest that change in habitat structure and resources levels could be important to take in consideration for the conservation of these forest birds.     

Mallards Feed Longer to Maintain Intake Rate under Competition on a Natural Food Distribution

Animals foraging in groups may benefit from a faster detection of food and predators, but competition by conspecifics may reduce intake rate. Competition may also alter the foraging behaviour of individuals, which can be influenced by dominance status and the way food is distributed over the environment. Many studies measuring the effects of competition and dominance status have been conducted on a uniform or highly clumped food distribution, while in reality prey distributions are often in‐between these two extremes. The few studies that used a more natural food distribution only detected subtle effects of interference and dominance. We therefore conducted an experiment on a natural food distribution with focal mallards Anas platyrhynchos foraging alone and in a group of three, having a dominant, intermediate or subordinate dominance status. In this way, the foraging behaviour of the same individual in different treatments could be compared, and the effect of dominance was tested independently of individual identity. The experiment was balanced using a 4 × 4 Latin square design, with four focal and six non‐focal birds. Individuals in a group achieved a similar intake rate (i.e. number of consumed seeds divided by trial length) as when foraging alone, because of an increase in the proportion of time feeding (albeit not significant for subordinate birds). Patch residence time and the number of different patches visited did not differ when birds were foraging alone or in a group. Besides some agonistic interactions, no differences in foraging behaviour between dominant, intermediate and subordinate birds were measured in group trials. Possibly group‐foraging birds increased their feeding time because there was less need for vigilance or because they increased foraging intensity to compensate for competition. This study underlines that a higher competitor density does not necessarily lead to a lower intake rate, irrespective of dominance status.     

Simple models of feeding with time and enery contstraints

We analyze how the foraging currencies "rate" (net energy gainper unit time) and "efficiency" (net energy gain per unit energyexpenditure) relate to the workload adopted by a forager. Weconsider feeding (gathering food for immediate consumption)as opposed to provisioning and investigate the influence oftime and energy constraints. In our model the forager may varythe level of energy expenditure while foraging; increased expenditureincreases the rate of gain, but with diminishing returns. Weshow that rate maximizing requires a higher rate of energy expenditurethan efficiency-maximizing, and we compare the performance ofrate- and efficiency-maximizing tactics when the feeding strategyis (1) to maximize the total net gain while foraging; (2) tomaximize the total net daily gain; or (3) to meet a requirement.Generally, the rate-maximizing tactic only performs best whentime is limiting; otherwise, a lighter workload and slower feedingrate perform better. Under the restricted conditions analyzedhere, no general statement can be made about the best tacticwhen the strategy is to meet a requirement. These results mayhelp explain several instances of "submaximal" foraging describedin the literature.     

Foraging tactics of a terrestrial salamander: Sustained yield in territories

Territorial red-backed salamanders (Plethodon cinereus) were given a high density of two prey types differing in size and caloric profitability. They chose a diet that approximated optimal foraging when they foraged in areas previously marked with advertisement pheromones. However, when foraging in previously unmarked or conspecific-marked areas they did not forage optimally, in a short time frame. In the latter two situations they evinced a lower rate of net energy due to their failure to specialize on the more profitable prey type and their longer intercapture intervals while time was devoted either to marking behaviour or submissive posturing. The salamanders appeared to opt for a strategy of sacrificing initial caloric yield until they had established marked territories and then switching to a higher sustained caloric yield. The data show that experimental handling of a predator per se can alter its foraging behaviour. Also a predator just initiating a territory may forage quite differently from one that has already established ownership, making the time frame during which observations are made important to understanding the predator's foraging strategy.     

Positive effect of predators on prey growth rate through induced modifications of prey behaviour

Many prey modify behaviour in response to predation risk and this modification frequently leads to a foraging rate reduction. Although this reduction can have a clear direct negative effect on prey growth rate, theory predicts that a net positive effect can occur when the combined reduction in foraging by the entire population leads to a large increase in resource level. Here, I present experimental results that corroborate this counterintuitive prediction: the predation threat of 'nonlethal' caged larval dragonflies ( Anax longipes ) caused a net increase in small bullfrog ( Rana catesbeiana ) growth. A behavioural response (i.e. a reduction in activity level and microhabitat usage) was likely to have negatively affected growth, but was offset by a positive effect on growth from a large increase in resource levels (measured using a bioassay). Further, the positive Anax effect was dependent on nutrient level, illustrating the role of the resource response magnitude. Results of this study are discussed in the context of studies in which Anax had the opposite (i.e. negative) effect on tadpole growth. Predator-induced modifications in prey behaviour can have large negative or positive effects on prey growth, the sign and magnitude of which are dependent on relative species density and resource dynamics.     

Incompletely informed shorebirds that face a digestive constraint maximize net energy gain when exploiting patches

Foragers that feed on hidden prey are uncertain about the intake rate they can achieve as they enter a patch. However, foraging success can inform them, especially if they have prior knowledge about the patch quality distribution in their environment. We experimentally tested whether and how red knots (Calidris canutus) use such information and whether their patch-leaving decisions maximized their long-term net energy intake rate. The results suggest that the birds combined patch sample information with prior knowledge by making use of the potential value assessment rule. We reject five alternative leaving rules. The potential encounter rate that the birds choose as their critical departure threshold maximized their foraging gain ratio (a modified form of efficiency) while foraging. The high experimental intake rates were constrained by rate of digestion. Under such conditions, maximization of the foraging gain ratio during foraging maximizes net intake rate during total time (foraging time plus digestive breaks). We conclude that molluscivore red knots, in the face of a digestive constraint, are able to combine prior environmental knowledge about patch quality with patch sample information to obtain the highest possible net intake over total time.     

Behavioural responses of cattle to shared foraging with wild herbivores in an East African rangeland

We assessed whether prior foraging by wild herbivores affected foraging behaviour of cattle in Laikipia rangeland, Kenya, during February 2001, August 2001 and February 2002. The study compared cattle bite rate, step rate and bites per step in plots exclusively accessible to cattle and those accessible to cattle and large wild herbivores. During February 2001 when conditions were dry, cattle bite rate was 18–19% lower, step rate 25–26% higher, and bites per step 36% lower in plots shared by cattle and wildlife compared to those exclusively accessible to cattle. Differences in these measured foraging behaviour parameters were strongly correlated with reductions in herbage cover in plots accessible to wild herbivores. Plot differences in herbage cover and the measured foraging behaviour parameters were not significant in the subsequent trials when conditions were wet, suggesting that wild herbivore impacts reported here are short-term within season and dependent on weather conditions (and plant productivity). With reduced herbaceous plant cover in wildlife grazed realms in the dry season, cattle respond with increased travel and reductions in bite rate and bites per step, suggesting that wild herbivores can seasonally affect foraging behaviour of cattle. It remains to be demonstrated whether or not these altered behaviours of cattle affect weight gains or other measures of performance.     

An energetic correlate between colony size and foraging effort in seabirds, an example of the Adélie penguin Pygoscelis adeliae

Central-place foraging seabirds alter the availability of their prey around colonies, forming a "halo" of reduced prey access that ultimately constrains population size. This has been indicated indirectly by an inverse correlation between colony size and reproductive success, numbers of conspecifics at other colonies within foraging range, foraging effort (i.e. trip duration), diet quality and colony growth rate. Although ultimately mediated by density dependence relative to food through intraspecific exploitative or interference competition, the proximate mechanism involved has yet to be elucidated. Herein, we show that Adélie penguin Pygoscelis adeliae colony size positively correlates to foraging trip duration and metabolic rate, that the metabolic rate while foraging may be approaching an energetic ceiling for birds at the largest colonies, and that total energy expended increases with trip duration although uncompensated by increased mass gain. We propose that a competition-induced reduction in prey availability results in higher energy expenditure for birds foraging in the halo around large colonies, and that to escape the halo a bird must increase its foraging distance. Ultimately, the total energetic cost of a trip determines the maximum successful trip distance, as on longer trips food acquired is used more for self maintenance than for chick provisioning. When the net cost of foraging trips becomes too high, with chicks receiving insufficient food, chick survival suffers and subsequent colony growth is limited. Though the existence of energetic studies of the same species at multiple colonies is rare, because foraging metabolic rate increases with colony size in at least two other seabird species, we suggest that an energetic constraint to colony size may generally apply to other seabirds.     

The effect of prey density on foraging mode selection in juvenile lumpfish: balancing food intake with the metabolic cost of foraging

1. In many species, individuals will alter their foraging strategy in response to changes in prey density. However, previous work has shown that prey density has differing effects on the foraging mode decisions of ectotherms as compared with endotherms. This is likely due to differences in metabolic demand; however, the relationship between metabolism and foraging mode choice in ectotherms has not been thoroughly studied. 2. Juvenile lumpfish Cyclopterus lumpus forage using one of two modes: they can actively search for prey while swimming, or they can 'sit-and-wait' for prey while clinging to the substrate using a ventral adhesive disk. The presence of these easily distinguishable foraging modes makes juvenile lumpfish ideal for the study of foraging mode choice in ectotherms. 3. Behavioural observations conducted during laboratory experiments showed that juvenile lumpfish predominantly use the 'cling' foraging mode when prey is abundant, but resort to the more costly 'swim' mode to seek out food when prey is scarce. The metabolic cost of active foraging was also quantified for juvenile lumpfish using swim-tunnel respirometry, and a model was devised to predict the prey density at which lumpfish should switch between the swim and cling foraging modes to maximize energy intake. 4. The results of this model do not agree with previous observations of lumpfish behaviour, and thus it appears that juvenile lumpfish do not try to maximize their net energetic gain. Instead, our data suggest that juvenile lumpfish forage in a manner that reduces activity and conserves space in their limited aerobic scope. This behavioural flexibility is of great benefit to this species, as it allows young individuals to divert energy towards growth as opposed to activity. In a broader context, our results support previous speculation that ectotherms often forage in a manner that maintains a minimum prey encounter rate, but does not necessarily maximize net energy gain.     

Energy regulation by traplining hummingbirds

1. A published model of constant diurnal energy accumulation by territorial hummingbirds does not accurately reflect the temporal distribution of feeding behaviour of traplining hummingbirds, Phaethornis longirostris (Long-Tailed Hermit Hummingbirds).
2. In an enclosure study, gross nectar intake by P . longirostris decreased through the day, mirroring nectar production rates in its natural food-flowers and mimicking its natural foraging patterns.
3. Using a simulation model, the energetic consequences of constant and decreasing net energy intake rates for traplining hummingbirds are compared.
4. Given natural patterns of nectar production, model birds with decreasing diurnal net intake rates met their energetic needs with fewer flowers than those with constant net intake, and spent less time foraging.
5. It is concluded that P . longirostris do not satisfy the physiological assumptions of the published model, and that in this way they are different from the territorial species on which the model has previously been tested.